Single-Cell Profiling and SCOPE-Seq Reveal Lineage Dynamics of Adult Ventricular-Subventricular Zone Neurogenesis and NOTUM as a Key Regulator

Cell Rep. 2020 Jun 23;31(12):107805. doi: 10.1016/j.celrep.2020.107805.

Abstract

In the adult ventricular-subventricular zone (V-SVZ), neural stem cells (NSCs) generate new olfactory bulb (OB) neurons and glia throughout life. To map adult neuronal lineage progression, we profiled >56,000 V-SVZ and OB cells by single-cell RNA sequencing (scRNA-seq). Our analyses reveal the molecular diversity of OB neurons, including fate-mapped neurons, lineage progression dynamics, and an NSC intermediate enriched for Notum, which encodes a secreted WNT antagonist. SCOPE-seq technology, which links live-cell imaging with scRNA-seq, uncovers cell-size transitions during NSC differentiation and preferential NOTUM binding to proliferating neuronal precursors. Consistently, application of NOTUM protein in slice cultures and pharmacological inhibition of NOTUM in slice cultures and in vivo demonstrated that NOTUM negatively regulates V-SVZ proliferation. Timely, context-dependent neurogenesis demands adaptive signaling among neighboring progenitors. Our findings highlight a critical regulatory state during NSC activation marked by NOTUM, which attenuates WNT-stimulated proliferation in NSC progeny.

Keywords: NOTUM; SCOPE-seq; WNT signaling; adult neural stem cell; lineage tracing; single cell RNA-sequencing; ventricular-subventricular zone.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging / metabolism*
  • Animals
  • Cell Lineage*
  • Cell Proliferation
  • Esterases / metabolism*
  • Gene Expression Regulation
  • Genes, Reporter
  • Lateral Ventricles / cytology*
  • Mice, Inbred C57BL
  • Neurogenesis*
  • Neurons / metabolism
  • Olfactory Bulb / cytology
  • Single-Cell Analysis*

Substances

  • Esterases
  • Notum protein, mouse